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Adherence to Physician Recommendations for Surveillance in Opportunistic Colorectal Cancer Screening: The Necessity of Organized Surveillance Christian Stock1,2*, Bernd Holleczek3, Michael Hoffmeister1, Thomas Stolz4, Christa Stegmaier3, Hermann Brenner1 1 Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany, 2 Institute of Medical Biometry and Informatics, University of Heidelberg, Heidelberg, Germany, 3 Saarland Cancer Registry, Saarbrücken, Germany, 4 Gastroenterologische Schwerpunktpraxis Völklingen, Kreppstraße 3-5, Völklingen, Germany

Abstract Background: Limited evidence exists on the utilization of surveillance colonoscopy in colorectal cancer (CRC) screening programs. We assessed adherence to physician recommendations for surveillance in opportunistic CRC screening in Germany. Methods: A follow-up study of screening colonoscopy participants in 2007-2009 in Saarland, Germany, was conducted using health insurance claims data. Utilization of additional colonoscopies through to 2011 was ascertained. Adherence to surveillance intervals of 3, 6, 12 and 36 months, defined as having had colonoscopy at 2.5 to 4, 5 to 8, 10.5 to 16 and 33 to 48 months, respectively (i.e., tolerating a delay of 33% of each interval) was assessed. Potential predictors of non-adherence were investigated using logistic regression analysis. Results: A total of 20,058 screening colonoscopy participants were included in the study. Of those with recommended surveillance intervals of 3, 6, 12 and 36 months, 46.5% (95%-confidence interval [CI]: 37.3-55.7%), 38.5% (95%-CI: 29.6-47.3%), 25.4% (95%-CI: 21.2-29.6%) and 28.0% (95%-CI: 25.5-30.5%), respectively, had a subsequent colonoscopy within the specified margins. Old age, longer recommended surveillance interval, not having had polypectomy at screening and negative colonoscopy were statistically significant predictors of non-adherence. Conclusion: This study suggests frequent non-adherence to physician recommendations for surveillance colonoscopy in community practice. Increased efforts to improve adherence, including introduction of more elements of an organized screening program, seem necessary to assure a high-quality CRC screening process. Citation: Stock C, Holleczek B, Hoffmeister M, Stolz T, Stegmaier C, et al. (2013) Adherence to Physician Recommendations for Surveillance in Opportunistic Colorectal Cancer Screening: The Necessity of Organized Surveillance. PLoS ONE 8(12): e82676. doi:10.1371/journal.pone.0082676 Editor: Jung Eun Lee, Sookmyung Women's University, Korea, Republic Of Received June 4, 2013; Accepted October 26, 2013; Published December 6, 2013 Copyright: © 2013 Stock et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The study was funded by the young scientists programme of the German network 'Health Services Research Baden-Württemberg' of the Ministry of Science, Research and Arts in collaboration with the Ministry of Employment and Social Order, Family, Women and Senior Citizens, BadenWürttemberg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. * E-mail: [email protected]

Introduction

approximately 20-30% of screening colonoscopies. It has been shown to be an effective tool for prevention of CRC if a good compliance is assured [2,3]. Current guidelines in the US and Germany distinguish between low-risk- and high-risk-adenoma situations in which the recommended surveillance interval is 3 years and 5 (to 10) years, respectively [4,5]. A shorter follow-up is needed in case of incomplete removal of adenomas or, independent of screening, due to signs and symptoms of gastrointestinal diseases. So far, only limited evidence exists on the actual utilization of surveillance colonoscopy in community practice. Studies conducted in the US reported overuse of surveillance

For slightly more than a decade, primary screening for colorectal cancer (CRC) by colonoscopy has been recommended and offered to the general population at average risk for CRC in the United States (US) and Germany. In both countries, screening colonoscopy is generally offered on an “opportunistic” basis, i.e. it depends on individuals to request screening or on their health advisors to recommend screening, and individuals are not invited from a centralized register [1]. Post-polypectomy surveillance using colonoscopy is an integral part of the CRC screening process and required after

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Data sources

colonoscopy particularly among low-risk individuals but also underuse among individuals with advanced findings at screening [6-9]. Some evidence also suggests that physicians tend to recommend colonoscopic surveillance more frequently than necessary according to guidelines [10-13]. Furthermore, the communication between endoscopists, primary care physicians and patients about results of screening colonoscopies and consequences for surveillance may often be suboptimal [11,14]. Very little evidence on the utilization of surveillance colonoscopy in community practice is available from the German healthcare system despite the introduction of colonoscopy as primary screening offer in 2002. Two recent studies suggested frequent utilization of additional colonoscopies along with substantial adenoma yield in the first 3 years after screening colonoscopy [15], and also substantial inter-physician variation in follow-up habits after screening colonoscopy [16]. In this study, we aimed to assess patient adherence to physician recommendations for surveillance in a follow-up period of up to 4 years after screening colonoscopy in the German opportunistic CRC screening program.

This study is based on health insurance claims and screening colonoscopy documentation data that were both routinely collected by the Regional Association of Statutory Health Insurance Physicians in Saarland between 2007 and 2011. The data cover all SHI funds in Saarland and thus reflect provision of services within the SHI system in the entire state. The screening colonoscopy documentation data used for the present study are required for physician reimbursement and were available in electronic format. Their contents follow a nationwide standard including information on completeness of the examination, macroscopic and histologic findings, polypectomies, acute complications, diagnoses and recommendations for further procedures. This documentation is routinely done for screening colonoscopies only, i.e., it is not available for colonoscopies performed for other indications.

Eligibility criteria Individuals insured by the SHI system and living in Saarland who underwent screening colonoscopy between 2007 and 2009 with and without subsequent recommendation for surveillance colonoscopy were eligible for inclusion in the study. Exclusion criteria were: (i) more than 1 screening colonoscopy coded in the claims data (indicates a coding error), (ii) no related screening colonoscopy documentation available, and (iii) CRC detected by the screening colonoscopy (entails special surveillance scheme after initial cancer treatment). Individuals without recommendation for surveillance were included to obtain information on the “baseline” utilization of further colonoscopy (most likely to be done for signs and symptoms of gastrointestinal disease) for comparison. If no surveillance is required, it is recommended to undergo a second screening colonoscopy after 10 years in the absence of other risk factors [4]. All individuals with screening colonoscopy in 2007 were followed-up for a minimum of 4 years through to 2011. Among individuals with screening colonoscopy in 2008 or 2009, utilization of further colonoscopies was only ascertained if physicians recommended short-term follow-up within ≤12 months in order to allow a minimum follow-up of one year in addition to the surveillance due date.

Methods A follow-up study of screening colonoscopy participants in Saarland, Germany, was conducted using statutory health insurance (SHI) claims and routine screening colonoscopy documentation data.

Ethics statement The study was approved by the data protection commissioner of Saarland and by the ethics committees of the University of Heidelberg and the Medical Association of Saarland. Anonymized data routinely collected by health insurances were analyzed. Written informed consent of patients was infeasible and not required by the approving institutional review board.

Setting Saarland is a federal state situated in the south-west of Germany with 1.01 million inhabitants in 2012, corresponding to 1.2% of the German population. In 2008, the age- and sexstandardized utilization of screening colonoscopy in Saarland was 2.9% (age range: 55-74 years), which was slightly higher than the average across all federal states in Germany of 2.4% [17]. Screening colonoscopy has been offered to the general population aged ≥55 years since October 2002 in the German SHI system which covers approximately 90% of the general population (similar offers are also made in the private sector) [18]. Only specialist physicians for internal medicine with subspecialization in gastroenterology or specialist physicians for colorectal surgery are entitled to perform screening colonoscopies and to receive reimbursement. They are required to perform at least 200 colonoscopies per year.

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Variables Utilization of colonoscopy was defined by health insurance claims for outpatient services according to the physician’s fee scale (Einheitlicher Bewertungsmaßstab [EBM]): “01741(M)” for screening colonoscopy and “13421(M)”, “13422(M)” for nonscreening colonoscopy. Deterministic encryption procedures were applied to personal identifiers (insurance codes) in the claims data and, in an analogous manner, to personal identifiers (insurance codes) in the screening documentation data. The analyst did not have access to personal information in plaintext stored in the insurance database and was unaware of the encryption procedure. Record linkage between multiple insurance claims for colonoscopy as well as between insurance claims for the initial screening colonoscopy and the respective

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Statistical methods

screening colonoscopy documentation was based on anonymized personal identifiers. Basic demographic characteristics (age, sex), information on indicators of process quality of the screening colonoscopy (sedation, cecal intubation, polypectomy, complications requiring intervention of the endoscopist), findings (number, size and histology of polyps) and recommendations on time to surveillance colonoscopy were drawn from the screening colonoscopy documentation. It is compulsory to provide information on whether and, if applicable, which further diagnostic or therapeutic procedures were recommended. The data did therefore not contain any missing values with respect to recommendations. Findings at screening were categorized as ‘negative’ (no adenomas, but including hyperplastic polyps), ‘low-risk adenoma’ (1-3 tubular adenomas, each

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